Euphorine phylogeny: the evolution of diversity in host-utilization by parasitoid wasps (Hymenoptera: Braconidae)

ABSTRACT.

• 1 New data on the phylogeny of the braconid subfamily Euphorinae supports the hypothesis that parasitism of adult insects by Euphorinae originated during parasitism of Chrysomelidae, a group whose larvae are ecologically coincident with adults.
• 2 Evolution of the habit of attacking the adult stage opened a new adaptive zone; subsequently the Euphorinae have diversified on to a phylogenetically greater variety of hosts than any other braconid subfamily.
• 3 Parasitism of eumastacid grasshoppers evolved from beetle parasitism in the tribe Perilitini.
• 4 The tribe Euphorini shows the greatest diversity of hosts utilized. Most attack Heteroptera; however, Chrysopopthorus diversified on to adult Chrysopidae, Euphoriella on to Psocoptera, and Cryptoxilos on to Scolytidae.
• 5 Parasitism of bark beetles (Scolytidae) has evolved independently in three genera: Cosmophorus, Cryptoxilos and Ropalophorus. This is the most specialized form of beetle parasitism by euphorines, since it involves direct parasitism of concealed hosts.
• 6 Parasitism of adult hymenopterans by the tribe Syntretini may be related to attacking hosts while they are foraging at flowers.
• 7 The pattern of diversification in the Euphorinae indicates several adaptive radiations within host orders, as well as a history of major host-shifts between phylogenetically distantly-related host groups: Coleoptera to Orthoptera; Coleoptera to Hymenoptera; Coleoptera to Heteroptera; Heteroptera to Neuroptera, Psocoptera, and back to Coleoptera. Both the‘host taxonomy’and‘host habitat’hypotheses of host-shifting are supported. Host-shifts have involved hosts occurring in the same micro-habitat and usually having similar feeding habits. This is consistent with current theory of host-location by means of host-produced kairomones and visual cues.

     

Physical and chemical cues influencing the oviposition behaviour of Aphidius ervi

The oviposition behaviour of the aphid parasitoid Aphidius ervi Haliday is influenced by both chemical and physical cues. Oviposition attack responses were elicited by paint pigments sealed into the tip of a glass capillary tube. Parasitoids reacted to yellow pigments with repeated oviposition attack responses, but they did not react to green pigments. The spectrum of reflected light from the yellow pigments was very similar to that from the `green' natural host Acyrthosiphon pisum (Harris), with a high proportion of the total radiation energy being emitted in the yellow-orange wavebands (580–660 nm). Pea aphid cornicle secretion also elicited oviposition attack responses, which were not exclusively induced by its pale yellow-green colour. In fact, the oviposition attack response to capillary tips coated with cornicle secretion remained evident under red light conditions, which, in contrast, nearly completely suppressed the response to yellow pigments. Chemical compounds from cornicle secretion do not appear to be involved in parasitoid orientation, even though they stimulate intense oviposition attack responses. Olfactometer experiments showed that the putative kairomone involved acts only at very short range or on contact. Host exuviae, which also elicited strong and persistent oviposition reactions from A. ervi females, appear to be a good alternative source of ovipositional kairomone(s). This work confirms the existence of an aphid cuticular kairomone.     

Host behaviour modification by the endoparasitoid Aphidius nigripes: a strategy to reduce hyperparasitism

Abstract. 1. One possible component of successful parasitism by insect parasitoids is the reduction of predation and hyperparasitism through the modification of host behaviour.
2. Just prior to death, potato aphids, Macrosiphum euphorbiae (Thomas), containing diapausing larvae of the parasitoid Aphidius nigripes Ashmead have been shown to leave the host plant to mummify in concealed sites, while those parasitized by non-diapausing individuals generally leave the aphid colony to mummify on the upper leaf surfaces.
3. The present study examines the within plant distribution of aphids and mummies containing non-diapausing A.nigripes , and compares parasitoid survival among microhabitats under field conditions.
4. On potato, Solunum tuberosum L., a significant proportion of aphids were found on lower leaf surfaces, whereas mummies were usually on the upper surfaces, particularly in the apical stratum of the plant canopy.
5. In both field surveys and experimental manipulations, parasitoid survival was higher on the upper surface of apical leaves than in other microhabitats, due to lower levels of hyperparasitism and, to a lesser extent, lower predation. This suggests that the pressure exerted by natural enemies has influenced the evolution of host behaviour modification.     

Feeding behaviour and phylogeny: observations on early derivative Acari

Based on laboratory observations of three species of Allothyrus (Parasitiformes: Holothyrida: Allothyridae) from south east Queensland and gut content analysis of 62 individuals representing 11 species of Allothyrus from eastern Australia, we determined that Australian Allothyridae are scavengers that ingest fluids only. Living arthropods, nematodes, snails and annelids were ignored, but dead arthropods were readily fed upon and were sufficient to maintain adults and nymphs for many months. The adults were sluggish, timid animals that relied on armour, thanatosis and probably on noxious chemicals for protection: the juveniles produced secretions from idiosomal glands. In contrast, most early derivative Mesostigmata that we tested (Sejina, species of Sejus and Uropodella; Uropodina, Polyaspis sp. and Cercomegistina, an undescribed Asternoseiidae) were aggressive predators of small invertebrates and ingested fluids only; however, two species of Asternolaelaps (Sejina) had solid fungal and animal material in their guts. Similarly, the early derivative acariform (Palaeosomata, species of Stomacarus and Loftacarus) and opilioacariform mites (an undescribed Opilioacarida from Australia) that we examined all ingested particulate foods, including fungal and animal material. These observations are consistent with the hypothesis that the earliest mites were scavengers and opportunistic predators that ingested solid foods and that fluid feeding is a derived condition linking the three orders of Parasitiformes (Holothyrida, Ixodida and Mesostigmata).     

Neurological influences on pheromone release and calling behaviour in the gypsy moth, Lymantria dispar

ABSTRACT. Surgical removal of the brain or disconnection of the last abdominal ganglion from the ventral nerve cord prevented sex pheromone release in female Lymantria dispar (L.) (Lymantriidae), as assayed by the male wing-fanning response. The calling behaviour continued to occur in individuals whose terminal abdominal ganglion had been thus isolated, however, indicating that the neural mechanisms controlling calling function independently in the last abdominal ganglion.     

Deuterium marking of chemical emissions: detectability and fitness consequences of a novel technique for insect behavioural studies

Behavioural studies often need to employ marking techniques to identify and track individuals. Marks ideally have no influence on behaviour or fitness of marked individuals or on the organisms with which they interact. A newly developed internal marking technique uses deuterium to manipulate the chemical emissions of bethylid wasps that are parasitoids of lepidopteran larvae. Wasps are deuterated indirectly by injecting deuterium oxide (heavy water) into the host on which they feed as larvae. Adult wasps emit a volatile chemical under stressful conditions and the emissions of deuterated and undeuterated wasps can be clearly and readily distinguished by measuring the ratio of deuterated/undeuterated molecules using real‐time mass spectrometry. Deuterated female wasps are, however, detectably disadvantaged in dyadic contests for host resources, a component of female fitness. In this study, we evaluated potential side‐effects of this deuterium marking technique on three further correlates of female Goniozus legneri Gordh (Hymenoptera: Bethylidae) fitness: longevity, lifetime fecundity, and offspring developmental mortality. We found that deuterium enrichment has no overall adverse effects on these parameters. We further showed that injecting hosts with different concentrations of deuterium results in distinguishably different volatile emissions of adult wasps, such that at least three individuals can be simultaneously identified by their chemical signatures. We also showed that deuterium marking remains effective beyond a wasp's death: deuterated and undeuterated wasps remain readily distinguishable after storage. We discuss potential applications of deuterium marking for the laboratory and field study of chemical communication, dispersal, and mating structure in parasitoid wasps and other insects.     

Chemistry of clitoral gland secretions of the laboratory rat: Assessment of behavioural response to identified compounds

The present investigations were carried out to find out the chemical nature of clitoral gland extracts and their involvement in reproductive and social behaviour. Homogenates of clitoral glands of mature estrous female rats were extracted with n-hexane and dichloromethane (1:1 ratio v/v) and analysed by gas chromatography linked mass spectrometry (GC-MS). Three peaks were found to be in higher concentration, which were identified as 6,11-dihydro-dibenz-b,e-oxepin-11-one (I); 2,6,10-dodecatrien-1-ol-3,7,11-trimethyl(Z) (II); and 1,2-benzene-dicarboxylic acid butyl(2-ethylpropyl) ester (III). Odour preference tests demonstrated that the first compound attracted conspecifics of the opposite sex. By contrast, the second and third compounds were found to attract both sexes. The results conclude that the clitoral gland of laboratory rat contains three major chemical compounds which have a unique function in maintaining social and reproductive status.     

A novel interference behaviour: invasive wasps remove ants from resources and drop them from a height

This study reports a novel form of interference behaviour between the invasive wasp Vespula vulgaris and the New Zealand native ant Prolasius advenus. By videotaping interactions at bait stations, we found that wasps commonly remove ant competitors from food resources by picking up the workers in their mandibles, flying backward and dropping them unharmed some distance from the food. Both the frequency and the efficiency of the wasp behaviour significantly increased with the abundance of ant competitors. Ant removals were the most common interference events initiated by wasps when ants were numerous, while intraspecific conflicts among wasps were prominent when few ants were present. The 'ant-dropping' behaviour emphasizes how asymmetry in body sizes between competitors can lead to a pronounced form of interference, related to asymmetric locomotion modes.     

Functional anatomy of haustoria formed by Rhinanthus minor: linking evidence from histology and isotope tracing

The root parasite Rhinanthus minor feeds on the xylem of a diverse range of species. Grasses and legumes are the best hosts, while on forbs R. minor typically shows poorer growth. It has been hypothesized that host quality is linked to the expression of defences against the parasite seen in forb roots, but never in grasses. The efficacy of these defence mechanisms in preventing resource loss has not, however, been measured directly. Here we combine histological characterization of haustoria formed on Cynosurus cristatus (a grass), Leucanthemum vulgare and Plantago lanceolata (forbs) with (15)N tracers supplied to the host to quantify the efficacy of these defence responses. Rhinanthus minor penetrated only the xylem of C. cristatus, abstracting an average of 17% of the (15)N tracer taken up, but only 2.5 and 0.2%, respectively, when attached to L. vulgare and P. lanceolata. For the first time, this study has established that the resistance mechanisms of the forbs are effective in preventing the parasite from directly accessing their xylem solutes.     

Within-patch foraging behaviour of the aphid parasitoidAphidius funebris: plant architecture, host behaviour, and individual variation

The influence of plant architecture, host colony size, and host colony structure on the foraging behaviour of the aphid parasitoidAphidius funebris Mackauer (Hymenoptera: Aphidiidae) was investigated using a factorial experimental design. The factorial design involved releasing individual parasitoid females in aphid colonies consisting of either 10 or 20 individuals ofUroleucon jaceae L. (Homoptera: Aphididae) of either only larval instar L3 or a mixture of host instars, both on unmanipulated plants and on plants that had all leaves adjacent to the colony removed. Interactions between the parasitoid and its host were recorded until the parasitoid had left the plant. The time females spent on the host plant and the number of eggs laid varied greatly among females. Host colony size significantly affected patch residence time and the number of contacts between parasitoids and aphids. Plant architecture influenced the time-budget of the parasitoids which used leaves adjacent to the aphid colony for attacking aphids. Female oviposition rate was higher on unmanipulated plants than on manipulated plants. No further significant treatment effects on patch residence time, the number of contacts, attacks or ovipositions were found. Oviposition success ofA. funebris was influenced by instar-specific host behaviour. Several rules-of-thumb proposed by foraging theory did not account for parasitoid patch-leaving behaviour.     

Effects of nitrogen supply on the anatomy and chemical composition of leaves of four grass species belonging to the genus Poa, as determined by image-processing analysis and pyrolysis–mass spectrometry

Previous experiments have shown that the anatomy and chemical composition of leaves of inherently fast- and slow-growing grass species, grown at non-limiting nitrogen supply, differ systematically. The present experiment was carried out to investigate whether these differences persist when the plants are grown at an intermediate or a very low nitrogen supply. To this end, the inherently fast-growing Poa annua L. and Poa trivialis L., and the inherently slow-growing Poa compressa L. and Poa pratensis (L.) Schreb. were grown hydroponically at three levels of nitrate supply: at optimum (RGR_max) and at relative addition rates of 100 and 50 mmol N (mol N)^?1 d^?1 (RAR₁₀₀ and RAR₅₀), respectively. As expected, at the lowest N supply, the potentially fast-growing species grew at the same rate as the inherently slow-growing ones. Similarly, the differences in leaf area ratio (LAR, leaf area:total dry mass), specific leaf area (SLA, leaf arear:leaf dry mass) and leaf mass ratio (LMR, leaf dry mass:total dry mass) disappeared. Under optimal conditions, the fast-growing species differed from the slow-growing ones in that they had a higher N concentration. There were no significant differences in C concentration. With decreasing N supply, the total N concentration decreased and the differences between the species disappeared. The total C concentration increased for the fast-growing species and decreased for the slow-growing ones, i.e. the small, but insignificant, difference in C concentration between the species at RGR_max increased with decreasing N supply. The chemical composition of the leaves at low N supply, analysed in more detail by pyrolysis–mass spectrometry, showed an increase in the relative amounts of guaiacyl lignin, cellulose and hemicellulose, whereas those of syringyl lignin and protein decreased. The anatomy and morphology of the leaves of the four grass species differing in RGR_max were analysed by image-processing analysis. The proportion of the total volume occupied by mesophyll plus intercellular spaces and epidermis did not correlate with the amount of leaf mass per unit leaf area (specific leaf mass, SLM) at different N supply. The higher SLM at low N supply was caused partly by a high proportion of non-veinal sclerenchymatic cells per cross-section and partly by the smaller volume of epidermal cells. We conclude that the decrease in relative growth rate (and increase in SLM) at decreasing N supply is partly due to chemical and anatomical changes. The differences between the fast- and slow-growing grass species at an optimum nutrient supply diminished when plants were growing at a limiting nitrogen supply.     

Volatile compounds from Liposcelis bostrychophila (Psocoptera: Liposcelididae) and their environment and their effects on settling behaviour

Headspace from above either Liposcelis bostrychophila Badonnel reared on powdered food; insects without food or from powdered food only were collected on five occasions over a period of four weeks. Volatiles were analysed by thermal desorption gas chromatography-mass spectrometry (TD-GCMS) to look for ecologically significant volatile compounds. Hexanoic acid (HA) was the major compound in the insect only and diet only volatiles (insect 25.6 ± 1.6%, diet 32.9 ± 1.13%). Isobutyric acid was the main compound detected in the volatiles from both insects and diet (35.3 ± 6%). Butyric acid (BA) and acetoin (HB) were also present at >2% of the total peak areas. HB was not detected in the insect only volatiles. Bioassays showed that hexanoic acid was the most repellent chemical. Mixtures of compounds representing the proportions of HA, BA, IBA, and HB in the volatiles did not have any prolonged effect on settling or selection by booklice in a two choice bioassay. L. bostrychophila can avoid individual volatile chemicals but the effects can be masked when they are incorporated into mixtures. As some volatile compounds can be detected by booklice they may govern dispersal, but further work is required to clarify their significance.     

Annexin A2/P11 interaction: new insights into annexin A2 tetramer structure by chemical crosslinking, high-resolution mass spectrometry, and computational modeling

During the past few years, the structural analysis of proteins and protein complexes by chemical crosslinking and mass spectrometry has enjoyed increasing popularity. With this approach we have investigated the quaternary structure of the complex between annexin A2 and p11, which is involved in numerous cellular processes. Although high-resolution data are available for both interaction partners as well as for the complex between two p11 subunits and two annexin A2 N-terminal peptides, the structure of the complete annexin A2/p11 heterotetramer has not yet been solved at high resolution. Thus, the quaternary structure of the biologically relevant, membrane-bound annexin A2/p11 complex is still under discussion, while the existence of a heterotetramer or a heterooctamer is the prevailing opinion. We gained further insight into the spatial organization of the annexin A2/p11 heterotetramer by employing chemical crosslinking combined with high-resolution mass spectrometry. Furthermore, tandem mass spectrometry served as a tool for an exact localization of crosslinked amino acid residues and for a confirmation of crosslinked product assignment. On the basis of distance constraints from the crosslinking data we derived structural models of the annexin A2/p11 heterotetramer by computational docking with Rosetta. We propose an octameric model for the annexin A2/p11 complex, which exerts annexin A2 function. The proposed structure of the annexin A2/p11 octamer differs from so far suggested models and sheds new light into annexin A2/p11 interaction.     

Egg predation within the nests of social wasps: a new genus and species of Phlaeothripidae,and evolutionary consequences of Thysanoptera invasive behaviour

The insects known as thrips are commonly thought of as flower‐living and pestiferous organisms, but we report here a novel interaction between a phlaeothripine thrips species, Mirothrips arbiter gen. et sp. nov. and three species of social paper wasps in Brazil. This thrips species breeds inside the wasp colonies, and larval and adult thrips feed on wasp eggs, which become severely damaged. Infested nests can contain up to 300 M. arbiter gen. et sp. nov. individuals. The closest relatives of M. arbiter are two presumably predaceous species: Mirothrips bicolor sp. nov. , which inhabits abandoned Cecidomyiidae galls, and Mirothrips analis comb. nov. , described from individuals collected in the silken bags of the caterpillars of Psychidae moths. The behaviour exhibited by M. arbiter represents one of the most evolutionarily advanced lifestyles known among Thysanoptera, and we predict that other polistine species serve as hosts for this thrips in Brazil. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 332–341.     

Species richness,abundance and diversity of ichneumonid wasps in Japanese beech forests impacted by sika deer and sawfly herbivory

We investigated the community structure of ichneumonid wasps inhabiting beech forests at six sites in the Tanzawa Mountains of Japan under different magnitudes of impact by sika deer Cervus nippon and beech sawfly Fagineura crenativora on vegetation. Using yellow flight-interception traps, we captured 2,528 ichneumonid wasps representing 367 species in 23 subfamilies. The number of species at each site ranged from 77 to 136 and approximately 80% of these were low-density species (i.e. only one to two individuals captured per site). The number of individuals at each site ranged from 248 to 897, and the percentage of the beech sawfly parasitoids varied widely from 1% to 57%. The numbers of species in parasitoid groups categorized according to their hosts, that is, sawfly (not including the beech sawfly), Lepidoptera, woodborer, fungivore or the others, did not greatly differ among the study sites. Parasitoids attacking herbivorous insects exceeded others in species richness and abundance at all sites. Six sites were classified into four groups in terms of abundance of the host groups when excluding the parasitoids of the beech sawfly, but into only two groups when including these parasitoids. Species diversity and evenness were the highest at the least impacted site even if the beech sawfly parasitoids were excluded from calculation. We suggested some environmental factors, such as groundcover vegetation, abundance of the beech sawfly and structure and age of forest stands, that could have affected the community structure of ichneumonid wasps in the beech forests.     

Host discrimination modulates brood guarding behaviour and the adaptive superparasitism in the parasitoid wasp Trissolcus semistriatus (Hymenoptera: Scelionidae)

Because hosts utilized by parasitoids are vulnerable to further oviposition by conspecifics, host guarding benefits female wasps. The present study aims to test whether female adults regulate brood guarding behaviour by host discrimination in a solitary parasitoid Trissolcus semistriatus by presenting an intact or parasitized host egg mass to a female adult. Virgin females without oviposition experience have host discrimination ability, which enables them to adjust the number of eggs laid in the hosts. Mating experience increases superparasitism by female adults, whereas mated females achieve a higher discrimination ability as a result of oviposition experience and show a lower superparasitism rate. As expected, females exhibit brood guard after parasitizing an intact host egg mass, whereas those females visiting a previously parasitized host egg mass, do not. Because the survival of eggs in superparasitized hosts is relatively low, regulating brood guarding behaviour by host discrimination is adaptive for female wasps.     

Observations on the anatomy,behaviour, reproduction and life cycle of the cubozoan Carybdea sivickisi

Substantial numbers of the very small carybdeid jellyfish, Carybdea sivickisi, have been observed feeding actively by divers in the vicinity of fringing coral reefs. During the day specimens were seen in close association with the substrate and with sessile macroalgae. They appeared able to adhere to substrates by contact with an area on the aboral surface of the bell. Individuals maintained in the laboratory showed the same adhering ability. The adhesive organs correspond to 4 areas of raised secretory epithelium on the aboral surface.Following capture, one isolated specimen extruded a long gelatinous strand containing several thousand developing embryos and numerous functional nematocysts. The embryos developed into characteristic cubozoan planulae, which were able to attach themselves temporarily to substrates by means of nematocysts. After 4 days of free swimming, planulae began to attach permanently and to develop into sessile polyps with 3 or 4 tentacles, each armed with a single stenotele.The species displays sexual dimorphism and evidence for spermatophore formation and transfer which parallel that reported for Tripedalia cystophora. The presence of sperm-storage sacs in both sexes, the production of an embryo mass, the adhering behaviour and an apparent association with algal substrates are among features apparently unique to the species.     

A new genus of xenophyophores (Foraminifera) from Japan Trench: morphological description,molecular phylogeny and elemental analysis

The deep‐sea floor is inhabited by a number of unusual and enigmatic taxa, unknown in shallow waters. These include the xenophyophores, a group of giant protists that construct fragile agglutinated tests. Here, we describe Shinkaiya lindsayi gen. et sp. nov. , a new xenophyophore collected by the submersible Shinkai 6500 at a depth of 5435 m near the Japan Trench. The phylogenetic analysis performed on its complete small‐subunit ribosomal DNA (SSU rDNA) sequence confirms that Sh. lindsayi sp. nov. is a foraminiferan that is closely related to another xenophyophore, Syringammina corbicula Richardson, 2001, and to a monothalamous (single‐chambered) foraminiferan Rhizammina algaeformis Brady, 1879. In terms of morphology, the new genus resembles Syringammina, but its test wall is thicker, softer, and more weakly cemented. Moreover, the SSU rDNA sequences of the two genera are highly divergent. Mass spectra analyses reveal unusually high concentrations of some elements, such as lead, uranium, and mercury. The granellare system (the cytoplasm and the organic sheath that encloses it) is apparently devoid of barite crystals, which are usually abundant as intracellular inclusions in xenophyophores, but is rich in mercury (with 12 times the concentration of mercury found in the surrounding sediment). Fecal pellets retained within a tubular system (stercomare) concentrate heavy metals, including lead and uranium (respectively, two and six times more than that of the sediment). Based on a comparison of the compositions of the agglutinated test wall, the granellare, the stercomare, and the surrounding sediment, we discuss the impact of xenophyophores on their habitat. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 156 , 455–464.     

Nonreductive chemical release of intact N-glycans for subsequent labeling and analysis by mass spectrometry

A novel strategy is proposed, using cost-saving chemical reactions to generate intact free reducing N-glycans and their fluorescent derivatives from glycoproteins for subsequent analysis. N-Glycans without core α-1,3-linked fucose are released in reducing form by selective hydrolysis of the N-type carbohydrate–peptide bond of glycoproteins under a set of optimized mild alkaline conditions and are comparable to those released by commonly used peptide-N-glycosidase (PNGase) F in terms of yield without any detectable side reaction (peeling or deacetylation). The obtained reducing glycans can be routinely derivatized with 2-aminobenzoic acid (2-AA), 1-phenyl-3-methyl-5-pyrazolone (PMP), and potentially some other fluorescent reagents for comprehensive analysis. Alternatively, the core α-1,3-fucosylated N-glycans are released in mild alkaline medium and derivatized with PMP in situ, and their yields are comparable to those obtained using commonly used PNGase A without conspicuous peeling reaction or any detectable deacetylation. Using this new technique, the N-glycans of a series of purified glycoproteins and complex biological samples were successfully released and analyzed by electrospray ionization mass spectrometry (ESI–MS) and tandem mass spectrometry (MS/MS), demonstrating its general applicability to glycomic studies.     

Antennal glands in Psylliodes chrysocephala, and their possible role in reproductive behaviour

Abstract. The antennal morphology of Psylliodes chrysocephala L. (Coleoptera: Chrysomelidae), an important pest of oilseed rape ( Brassica napus ), was studied. Two types of tricellular, integumentary glands were found. The common antennal glands are distributed under all sensilla-bearing parts of male and female antennae. The male-specific antennal glands are only located under a glabrous area found on antennomeres 6–10 of male beetles. The common antennal glands are synthetically active in both pre- and post-diapause adults, but the male specific antennal glands are only active in post-diapause (reproductively active) males. During studies of mating behaviour, the antennae of the males were highly active at the beginning and end of copulation, and in response to increased female activity. The male specific antennal glands may secrete a sex pheromone, and the glabrous area on the male antennae could be the release site for such a pheromone.